Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone

Journal of Neuroscience

Volumn 28, Issue 11, 2008, Pages 2903-2911

  Chen, Yuncai ^a   Dubé, Céline M ^a   Rice, Courtney J ^a   Baram, Tallie Z ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Actin; CRF; CRH; Dendritic spine; Hippocampus; Stress; Synaptic plasticity; Two photon

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC STRESS; CONTROLLED STUDY; DENDRITIC SPINE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPINAL CORD ATROPHY; STRESS;

ANIMALS; CELL COUNT; CORTICOTROPIN-RELEASING HORMONE; DENDRITIC SPINES; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICE, TRANSGENIC; ORGAN CULTURE TECHNIQUES; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; STRESS; TIME FACTORS;

EID: 40849141136     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0225-08.2008     Document Type: Article

References (60)

1. Alfarez D, Joels M, Krugers H (2003) Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur J Neurosci 17:1928-1934.
2. Arancio O, Chao MV (2007) Neurotrophins, synaptic plasticity and dementia. Curr Opin Neurobiol 17:325-330.
3. Armstrong DD (2001) Rett syndrome: neuropathology (2000). Brain Dev 23:S72-S76.
4. Augustine GJ, Santamaria F, Tanaka K (2003) Local calcium signaling in neurons. Neuron 40:331-346.
5. Bamburg JR (1999) Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu Rev Cell Dev Biol 15:185-230.
6. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
7. Brunson KL, Eghbal-Ahmadi M, Bender R, Chen Y, Baram TZ (2001) Long-term progressive hippocampal cell loss and dysfunction induced by early-life administration of corticotropin releasing hormone reproduce the effects of early-life stress. Proc Natl Acad Sci USA 98:8856-8861.
8. Brunson KL, Kramar E, Lin B, Chen Y, Colgin LL, Yanagihara TK, Lynch G, Baram TZ (2005) Mechanisms of late-onset cognitive decline after early-life stress. J Neurosci 25:9328-9338.
9. Calabrese B, Halpain S (2005) Essential role for the PKC target MARCKS in maintaining dendritic spine morphology. Neuron 48:77-90.
10. Chalmers DT, Lovenberg TW, De Souza EB (1995) Localization of novel corticotropin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1 receptor mRNA expression. J Neurosci 15:6340-6350.
11. Chen LY, Rex CS, Casale MS, Gall CM, Lynch G (2007) Changes in synaptic morphology accompany actin signaling during LTP. J Neurosci 27:5363-5372.
12. 1)-like immunoreactivity in the mouse brain: light microscopy analysis using an antibody directed against the C-terminus. J Comp Neurol 420:305-323.
13. Chen Y, Bender RA, Frotscher M, Baram TZ (2001) Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: a quantitative spatiotemporal analysis. J Neurosci 21:7171-7181.
14. Chen Y, Bender RA, Brunson KL, Pomper JK, Grigoriadis DE, Wurst W, Baram TZ (2004a) Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proc Natl Acad Sci USA 101:15782-15787.
15. Chen Y, Brunson KL, Adelmann G, Bender RA, Frotscher M, Baram TZ (2004b) Hippocampal corticotropin releasing hormone: pre- and postsynaptic location and release by stress. Neuroscience 126:533-540.
16. Chen Y, Fenoglio KA, Dube CM, Grigoriadis DE, Baram TZ (2006) Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent. Mol Psychiatry 11:992-1002.
17. De Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463-475.
18. Donohue HS, Gabbott PL, Davies HA, Rodríguez JJ, Cordero MI, Sandi C, Medvedev NI, Popov VI, Colyer FM, Peddie CJ, Stewart MG (2006) Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: a stereological and three-dimensional ultrastructural study. Neuroscience 140:597-606.
19. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70.
20. Ethell IM, Pasquale EB (2005) Molecular mechanisms of dendritic spine development and remodeling. Prog Neurobiol 75:161-205.
21. Fenoglio KA, Chen Y, Baram TZ (2006) Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J Neurosci 26:2434-2442.
22. Fu WY, Chen Y, Sahin M, Zhao XS, Shi L, Bikoff JB, Lai KO, Yung WH, Fu AK, Greenberg ME, Ip NY (2007) Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat Neurosci 10:67-76.
23. Govek EE, Newey SE, Van Aelst L (2005) The role of the Rho GTPases in neuronal development. Genes Dev 19:1-49.
24. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509-514.
25. Hering H, Sheng M (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2:880-888.
26. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279-291.
27. Holtzman J (2007) Disparities in adverse birth outcomes may reflect influence of stress. Am J Public Health 97:1541.
28. Kennedy MB, Beale HC, Carlisle HJ, Washburn LR (2005) Integration of biochemical signalling in spines. Nat Rev Neurosci 6:423-434.
29. Khan S, Milot M, Lecompte-Collin J, Plamondon H (2004) Time-dependent changes in CRH concentrations and release in discrete brain regions following global ischemia: effects of MK-801 pretreatment. Brain Res 1016:48-57.
30. Kim J, Diamond D (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453-462.
31. Koester HJ, Sakmann B (1998) Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc Natl Acad Sci USA 95:9596-9601.
32. Lin B, Kramar EA, Bi X, Brucher FA, Gall CM, Lynch G (2005) Theta stimulation polymerizes actin in dendritic spines of hippocampus. J Neurosci 25:2062-2069.
33. Magarinos A, McEwen BS (1995) Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69:89-98.
34. Mainen ZF, Malinow R, Svoboda K (1999) Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature 399:151-155.
35. Maletic-Savatic M, Malinow R, Svoboda K (1999) Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283:1923-1927.
36. McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122.
37. McGill BE, Bundle SF, Yaylaoglu MB, Carson JP, Thaller C, Zoghbi HY (2006) Enhanced anxiety and stress-induced corticosterone release are associated with increased Crh expression in a mouse model of Rett syndrome. Proc Natl Acad Sci USA 103:18267-18272.
38. Merali Z, McIntosh J, Kent P, Michaud D, Anisman H (1998) Aversive and appetitive events evoke the release of corticotropin-releasing hormone and bombesin-like peptides at the central nucleus of the amygdala. J Neurosci 18:4758-4766.
39. Nägerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T (2004) Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44:759-767.
40. Nemeroff CB (2004) Early-life adversity, CRF dysregulation, and vulnerability to mood and anxiety disorders. Psychopharmacol Bull 38:14-20.
41. Okamoto K, Nagai T, Miyawaki A, Hayashi Y (2004) Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112.
42. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM, Ehlers MD (2006) Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52:817-830.
43. Pawlak R, Rao BS, Melchor JP, Chattarji S, McEwen B, Strickland S (2005) Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc Natl Acad Sci USA 102:18201-18206.
44. Penzes P, Beeser A, Chernoff J, Schiller MR, Eipper BA, Mains RE, Huganir RL (2003) Rapid induction of dendritic spine morphogenesis by transsynaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37:263-274.
45. Preil J, Muller MB, Gesing A, Reul JM, Sillaber I, van Gaalen MM, Landgrebe J, Holsboer F, Stenzel-Poore M, Wurst W (2001) Regulation of the hypothalamic-pituitary-adrenocortical system in mice deficient for CRH receptors 1 and 2. Endocrinology 142:4946-4955.
46. Radley JJ, Rocher AB, Miller M, Janssen WG, Liston C, Hof PR, McEwen BS, Morrison JH (2006) Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb Cortex 16:313-320.
47. Roelandse M, Matus A (2004) Hypothermia-associated loss of dendritic spines. J Neurosci 24:7843-7847.
48. Roman F, Staubli U, Lynch G (1987) Evidence for synaptic potentiation in a cortical network during learning. Brain Res 418:221-226.
49. Sapolsky RM (2000) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57:925-935.
50. Schierhorn H (1981) Structural change in neocortical pyramidal neurons in man in the 5th to 9th decade. Psychiatr Neurol Med Psychol 33:664-673.
51. Schubert V, Da Silva JS, Dotti CG (2006) Localized recruitment and activation of RhoA underlies dendritic spine morphology in a glutamate receptor-dependent manner. J Cell Biol 172:453-467.
52. Segal M (2005) Dendritic spines and long-term plasticity. Nat Rev Neurosci 6:277-284.
53. Sfakianos MK, Eisman A, Gourley SL, Bradley WD, Scheetz AJ, Settleman J, Taylor JR, Greer CA, Williamson A, Koleske AJ (2007) Inhibition of Rho via Arg and p190RhoGAP in the postnatal mouse hippocampus regulates dendritic spine maturation, synapse and dendrite stability, and behavior. J Neurosci 27:10982-10992.
54. Swanson LW, Sawchenko PE, Rivier J, Vale WW (1983) Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36:165-186.
55. Swinny JD, Valentino RJ (2006) Corticotropin-releasing factor promotes growth of brain norepinephrine neuronal processes through Rho GTPase regulators of the actin cytoskeleton in rat. Eur J Neurosci 24:2481-2490.
56. Tada T, Sheng M (2006) Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 16:95-101.
57. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, Sawchenko PE (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428:191-212.
58. Woolley CS, Gould E, Frankfurt M, McEwen BS (1990) Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039.
59. Yuste R, Bonhoeffer T (2004) Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5:24-34.
60. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757.